The Polycomb protein LHP1 regulates Arabidopsis thaliana stress responses through the repression of the MYC2-dependent branch of immunity.
Abscisic Acid
/ metabolism
Animals
Aphids
Arabidopsis
/ genetics
Arabidopsis Proteins
/ genetics
Basic Helix-Loop-Helix Leucine Zipper Transcription Factors
/ metabolism
Cyclopentanes
Ethylenes
/ metabolism
Gene Expression Regulation, Plant
Oxylipins
Plant Diseases
/ immunology
Plant Immunity
/ immunology
Polycomb-Group Proteins
Pseudomonas syringae
/ metabolism
Salicylic Acid
/ metabolism
Transcription Factors
/ genetics
Transcriptome
H3K27me3
LHP1
MYC2
Polycomb
abscisic acid
aphid
drought
pathogen
salicylic acid
stress
Journal
The Plant journal : for cell and molecular biology
ISSN: 1365-313X
Titre abrégé: Plant J
Pays: England
ID NLM: 9207397
Informations de publication
Date de publication:
12 2019
12 2019
Historique:
received:
28
05
2019
revised:
26
07
2019
accepted:
01
08
2019
pubmed:
23
8
2019
medline:
28
7
2020
entrez:
23
8
2019
Statut:
ppublish
Résumé
Polycomb repressive complexes (PRCs) have been traditionally associated with the regulation of developmental processes in various organisms, including higher plants. However, similar to other epigenetic regulators, there is accumulating evidence for their role in the regulation of stress and immune-related pathways. In the current study we show that the PRC1 protein LHP1 is required for the repression of the MYC2 branch of jasmonic acid (JA)/ethylene (ET) pathway of immunity. Loss of LHP1 induces the reduction in H3K27me3 levels in the gene bodies of ANAC019 and ANAC055, as well as some of their targets, leading to their transcriptional upregulation. Consistently, increased expression of these two transcription factors leads to the misregulation of several of their genomic targets. The lhp1 mutant mimics the MYC2, ANAC019, and ANAC055 overexpressers in several of their phenotypes, including increased aphid resistance, abscisic acid (ABA) sensitivity and drought tolerance. In addition, like the MYC2 and ANAC overexpressers, lhp1 displays reduced salicylic acid (SA) content caused by a deregulation of ICS1 and BSMT1, as well as increased susceptibility to the hemibiotrophic pathogen Pseudomonas syringae pv. tomato DC3000. Together, our results indicate that LHP1 regulates the expression of stress-responsive genes as well as the homeostasis and responses to the stress hormones SA and ABA. This protein emerges as a key chromatin player fine tuning the complex balance between developmental and stress-responsive processes.
Substances chimiques
ANAC019 protein, Arabidopsis
0
ANAC055 protein, Arabidopsis
0
Arabidopsis Proteins
0
Basic Helix-Loop-Helix Leucine Zipper Transcription Factors
0
Cyclopentanes
0
Ethylenes
0
LHP1 protein, Arabidopsis
0
MYC2 protein, Arabidopsis
0
Oxylipins
0
Polycomb-Group Proteins
0
Transcription Factors
0
jasmonic acid
6RI5N05OWW
Abscisic Acid
72S9A8J5GW
ethylene
91GW059KN7
Salicylic Acid
O414PZ4LPZ
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1118-1131Informations de copyright
© 2019 The Authors The Plant Journal © 2019 John Wiley & Sons Ltd.
Références
Abe, H., Urao, T., Ito, T., Seki, M. and Shinozaki, K. (2003a) Arabidopsis AtMYC2 (bHLH) and AtMYB2 (MYB) function as transcriptional activators in abscisic acid signaling. Plant Cell, 15, 63-78.
Abe, H., Urao, T., Ito, T., Seki, M. and Shinozaki, K. (2003b) Transcriptional activators in abscisic acid signaling. Society, 15, 63-78.
Ariel, F., Jegu, T., Latrasse, D., Romero-Barrios, N., Christ, A., Benhamed, M. and Crespi, M. (2014) Noncoding transcription by alternative rna polymerases dynamically regulates an auxin-driven chromatin loop. Mol. Cell, 55, 383-396.
Bent, A.F. and Mackey, D. (2007) Elicitors, effectors, and R genes: the new paradigm and a lifetime supply of questions. Annu. Rev. Phytopathol. 45, 399-436.
Bigeard, J., Colcombet, J. and Hirt, H. (2015) Signaling mechanisms in pattern-triggered immunity (PTI). Mol. Plant, 8, 521-539.
Boller, T. and Felix, G. (2009) A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. Annu. Rev. Plant Biol. 60, 379-406.
Bratzel, F., López-Torrejón, G., Koch, M., Pozo, J.C. Del and Calonje, M. (2010) Keeping cell identity in Arabidopsis requires PRC1 RING-finger homologs that catalyze H2A monoubiquitination. Curr. Biol. 20, 1853-1859.
Bu, Q., Jiang, H., Li, C.B.C., Zhai, Q., Zhang, J., Wu, X., Sun, J., Xie, Q. and Li, C.B.C. (2008) Role of the Arabidopsis thaliana NAC transcription factors ANAC019 and ANAC055 in regulating jasmonic acid-signaled defense responses. Cell Res. 18, 756-767.
Cao, F.Y., Yoshioka, K. and Desveaux, D. (2011) The roles of ABA in plant-pathogen interactions. J. Plant. Res. 124, 489-499.
Chen, F., D'Auria, J.C., Tholl, D., Ross, J.R., Gershenzon, J., Noel, J.P. and Pichersky, E. (2003) An Arabidopsis thaliana gene for methylsalicylate biosynthesis, identified by a biochemical genomics approach, has a role in defense. Plant J. 36, 577-588.
Chen, Y., Wei, J., Wang, M., Shi, Z., Gong, W. and Zhang, M. (2012) The Crystal structure of Arabidopsis VSP1 reveals the plant class C-Like phosphatase structure of the DDDD superfamily of phosphohydrolases. PLoS ONE, 7, e49421.
Croce, L.Di and Helin, K. (2013) Transcriptional regulation by Polycomb group proteins. Nat. Struct. Mol. Biol. 20, 1147-1155.
Derkacheva, M., Steinbach, Y., Wildhaber, T., Mozgová, I., Mahrez, W., Nanni, P., Bischof, S., Gruissem, W. and Hennig, L. (2013) Arabidopsis MSI1 connects LHP1 to PRC2 complexes. EMBO J. 5, 1-13.
Ding, B. and Wang, G.-L. (2015) Chromatin versus pathogens: the function of epigenetics in plant immunity. Front. Plant Sci. 6, 675.
Dombrecht, B., Xue, G.P., Sprague, S.J. et al. (2007) MYC2 differentially modulates diverse Jasmonate-dependent functions in Arabidopsis. Plant Cell Online, 19, 2225-2245.
Edwards, K., Johnstone, C. and Thompson, C. (1991) A simple and rapid method for the preparation of plant genomic DNA for PCR analysis. Nucleic Acids Res. 19, 1349.
Ellis, C., Karafyllidis, I. and Turner, J.G. (2002) Constitutive activation of jasmonate signaling in an Arabidopsis mutant correlates with enhanced resistance to Erysiphe cichoracearum, Pseudomonas syringae, and Myzus persicae. Mol. Plant-Microbe Interact. 15, 1025-1030.
Endoh, M., Endo, T.A., Endoh, T. et al. (2012) Histone H2A mono-ubiquitination is a crucial step to mediate PRC1-dependent repression of developmental genes to maintain ES cell identity D. PLoS Genet. 8, e1002774.
Espinas, N.A., Saze, H. and Saijo, Y. (2016) Epigenetic control of defense signaling and priming in plants. Front. Plant Sci. 7, 1-7.
Gaudin, V., Libault, M., Pouteau, S., Juul, T., Zhao, G., Lefebvre, D. and Grandjean, O. (2001) Mutations in LIKE HETEROCHROMATIN PROTEIN 1 affect flowering time and plant architecture in Arabidopsis. Development, 128, 4847-4858.
Halim, V.A., Vess, A., Scheel, D. and Rosahl, S. (2006) The role of salicylic acid and jasmonic acid in pathogen defence. Plant Biol. 8, 307-313.
Huot, B., Yao, J., Montgomery, B.L. and He, S.Y. (2014) Growth-defense tradeoffs in plants: a balancing act to optimize fitness. Mol. Plant, 7, 1267-1287.
Jacobs, J.J., Kieboom, K., Marino, S., DePinho, R.A. and van Lohuizen, M. (1999) The oncogene and Polycomb-group gene bmi-1 regulates cell proliferation and senescence through the ink4a locus. Nature, 397, 164-168.
Jaouannet, M., Morris, J.A., Hedley, P.E. and Bos, J.I.B. (2015) Characterization of Arabidopsis transcriptional responses to different aphid species reveals genes that contribute to host susceptibility and non-host resistance. PLoS Pathog. 11, 1-26.
Jiang, H., Li, H., Bu, Q. and Li, C. (2009) The RHA2a-interacting proteins ANAC019 and ANAC055 may play a dual role in regulating ABA response and jasmonate response. Plant Signal. Behav. 4, 464-466.
Kassis, J.A., Kennison, J.A. and Tamkun, J.W. (2017) Polycomb and trithorax group genes in Drosophila. Genetics, 206, 1699-1725.
Kazan, K. and Manners, J.M. (2013) MYC2: the master in action. Mol. Plant, 6, 686-703.
Kim, J.H., Durrett, T.P., Last, R.L. and Jander, G. (2004) Characterization of the Arabidopsis TU8 glucosinolate mutation, an allele of TERMINAL FLOWER2. Plant Mol. Biol. 54, 671-682.
Kulkarni, S.R., Vaneechoutte, D., Van de Velde, J. and Vandepoele, K. (2017) TF2Network: predicting transcription factor regulators and gene regulatory networks in Arabidopsis using publicly available binding site information. Nucleic Acids Res. 46, e31-e31.
Lämke, J. and Bäurle, I. (2017) Epigenetic and chromatin-based mechanisms in environmental stress adaptation and stress memory in plants. Genome Biol. 18, 124.
Lewis, E.B. (1978) A gene complex controlling segmentation in Drosophila. Nature, 276, 565-570.
Lievens, L., Pollier, J., Goossens, A., Beyaert, R. and Staal, J. (2017) Abscisic acid as pathogen effector and immune regulator. Front. Plant Sci. 8, 1-15.
Liu, Y., Ahn, J., Datta, S. et al. (2005) Arabidopsis vegetative storage protein is an anti-insect acid phosphatase. Plant Physiol. 139, 1545-1556.
Liu, C., Cheng, J., Zhuang, Y., Ye, L., Li, Z., Wang, Y., Qi, M. and Zhang, Y. (2018) Polycomb repressive complex 2 attenuates ABA-induced senescence in Arabidopsis. Plant J. 97, 368-377.
Lorenzo, O., Chico, J., Sánchez-Serran, J. and Solano, R. (2004) JASMONATE-INSENSITIVE1 encodes a MYC transcription factor essential to discriminate between different jasmonate-regulated defense responses in Arabidopsis. Plant Cell, 16, 1938-1950.
Ludwig-Muller, J., Pieper, K., Ruppel, M., Cohen, J.D., Epstein, E., Kiddle, G. and Bennett, R. (1999) Indole glucosinolate and auxin biosynthesis in Arabidopsis thaliana (L.) Heynh. glucosinolate mutants and the development of clubroot disease. Planta, 208, 409-419.
Mehta, S., Jeffrey, K.L., Unit, G. and Hospital, G. (2015) Beyond receptors and signaling: epigenetic factors in the regulation of innate immunity. Immunol. Cell Biol. 93, 233-244.
Merini, W., Romero-Campero, F.J., Gómez-Zambrano, A., Zhou, Y., Turck, F. and Calonje, M. (2017) The Arabidopsis polycomb repressive complex 1 (PRC1) components AtBMI1A, B, and C affect gene networks throughout all stages of plant development. Plant Physiol. 173, 627-641.
Mine, A., Berens, M.L., Nobori, T., Anver, S., Fukumoto, K., Winkelmüller, T.M., Takeda, A., Becker, D. and Tsuda, K. (2017) Pathogen exploitation of an abscisic acid- and jasmonate-inducible MAPK phosphatase and its interception by Arabidopsis immunity. Proc. Natl Acad. Sci. 114, 7456-7461.
Molitor, A., Latrasse, D., Zytnicki, M. et al. (2016) The Arabidopsis hnRNP-Q Protein LIF2 and the PRC1 subunit LHP1 function in concert to regulate the transcription of stress-responsive genes. Plant Cell, 28, 2197-2211.
Nakahigashi, K., Jasencakova, Z., Schubert, I. and Goto, K. (2005) The Arabidopsis HETEROCHROMATIN PROTEIN1 homolog (TERMINAL FLOWER2) silences genes within the euchromatic region but not genes positioned in heterochromatin. Plant Cell Physiol. 46, 1747-1756.
Nürnberger, T. and Brunner, F. (2002) Innate immunity in plants and animals: emerging parallels between the recognition of general elicitors and pathogen-associated molecular patterns. Curr. Opin. Plant Biol. 5, 318-324.
Oberschall, A., Deák, M., Török, K., Sass, L., Vass, I., Kovács, I., Fehér, A., Dudits, D. and Horváth, G.V. (2000) A novel aldose/aldehyde reductase protects transgenic plants against lipid peroxidation under chemical and drought stresses. Plant J. 24, 437-446.
Ohto, M., Goto, K., Takada, S., Nakahigashi, K., Kotake, T., Takada, S., Nakahigashi, K., Ohto, M. and Goto, K. (2003) Arabidopsis TERMINAL FLOWER 2 gene encodes a heterochromatin protein 1 homolog and represses both FLOWERING LOCUS T to regulate flowering time and several floral homeotic genes. Plant Cell Physiol. 44, 555-564.
Probst, A.V. and Mittelsten Scheid, O. (2015) Stress-induced structural changes in plant chromatin. Curr. Opin. Plant Biol. 27, 8-16.
Rajasekhar, V.K. and Begemann, M. (2007) Concise review: roles of polycomb group proteins in development and disease: a stem cell perspective. Stem Cells, 25, 2498-2510.
Ramirez-Prado, J.S., Abulfaraj, A.A., Rayapuram, N. and Benhamed, M. (2018a) Plant immunity: from signaling to epigenetic control of defense. Trends Plant Sci. 23, 833-844.
Ramirez-Prado, J.S., Piquerez, S.J.M., Bendahmane, A., Hirt, H., Raynaud, C. and Benhamed, M. (2018b) Modify the histone to win the battle: chromatin dynamics in plant-pathogen interactions. Front. Plant Sci. 9, 355.
Rizzardi, K., Landberg, K., Nilsson, L., Ljung, K. and Sundãs-Larsson, A. (2011) TFL2/LHP1 is involved in auxin biosynthesis through positive regulation of YUCCA genes. Plant J. 65, 897-906.
Ross, A. and Somssich, I.E. (2016) A DNA-based real-time PCR assay for robust growth quantification of the bacterial pathogen Pseudomonas syringae on Arabidopsis thaliana. Plant Methods, 12, 1-8.
Le Roux, C., Prete, S. Del, Boutet-Mercey, S., Perreau, F., Balagué, C., Roby, D., Fagard, M. and Gaudin, V. (2014) The hnRNP-Q protein LIF2 participates in the plant immune response. PLoS ONE, 9, e99343.
Roy, S., Gupta, P., Rajabhoj, M.P., Maruthachalam, R. and Nandi, A.K. (2018) The polycomb-group repressor MEDEA attenuates pathogen defense. Plant Physiol. 177, 1728-1742.
Sanchez-Pulido, L., Devos, D., Sung, Z.R. and Calonje, M. (2008) RAWUL: a new ubiquitin-like domain in PRC1 Ring finger proteins that unveils putative plant and worm PRC1 orthologs. BMC Genom. 9, 308.
Santner, A. and Estelle, M. (2007) The JAZ proteins link jasmonate perception with transcriptional changes. Plant Cell Online, 19, 3839-3842.
Schmitz, J., Rossoni, A.W. and Maurino, V.G. (2018) Dissecting the physiological function of plant glyoxalase I and glyoxalase I-like proteins. Front. Plant Sci. 9, 1-7.
Schwartz, Y.B. and Pirrotta, V. (2013) A new world of Polycombs: unexpected partnerships and emerging functions. Nat. Rev. Genet. 14, 853-864.
Schwartz, Y.B. and Pirrotta, V. (2014) Ruled by ubiquitylation: a new order for polycomb recruitment. Cell Rep. 8, 321-325.
Singla-Pareek, S.L., Reddy, M.K. and Sopory, S.K. (2003) Genetic engineering of the glyoxalase pathway in tobacco leads to enhanced salinity tolerance. Proc. Natl Acad. Sci. 100, 14672-14677.
Smale, S.T., Tarakhovsky, A. and Natoli, G. (2014) Chromatin contributions to the regulation of innate immunity. Annu. Rev. Immunol. 32, 489-511.
Song, S., Huang, H., Gao, H. et al. (2014) Interaction between MYC2 and ETHYLENE INSENSITIVE3 modulates antagonism between jasmonate and ethylene signaling in Arabidopsis. Plant Cell, 26, 263-279.
Takada, S. and Goto, K. (2003) Terminal flower2, an Arabidopsis homolog of heterochromatin protein1, counteracts the activation of flowering locus T by constans in the vascular tissues of leaves to regulate flowering time. Plant Cell, 15, 2856-2865.
Terranova, R., Yokobayashi, S., Stadler, M.B., Otte, A.P., van Lohuizen, M., Orkin, S.H. and Peters, A.H.F.M. (2008) Polycomb group proteins Ezh2 and Rnf2 direct genomic contraction and imprinted repression in early mouse embryos. Dev. Cell, 15, 668-679.
Tran, L.-S.P. (2004) Isolation and functional analysis of Arabidopsis stress-inducible NAC transcription factors that bind to a drought-responsive cis-element in the early responsive to dehydration stress 1 promoter. Plant Cell Online, 16, 2481-2498.
Turck, F., Roudier, F., Farrona, S. et al. (2007) Arabidopsis TFL2/LHP1 specifically associates with genes marked by trimethylation of histone H3 lysine 27. PLoS Genet. 3, 0855-0866.
Tuteja, N. (2007) Abscisic acid and abiotic stress signaling. Plant Signal. Behav. 2, 135-138.
Veluchamy, A., Jegu, T., Ariel, F. et al. (2016) LHP1 regulates H3K27me3 spreading and shapes the three-dimensional conformation of the Arabidopsis genome M. PLoS ONE, 11, e0158936.
Walley, J.W., Rowe, H.C., Xiao, Y., Chehab, E.W., Kliebenstein, D.J., Wagner, D. and Dehesh, K. (2008) The chromatin remodeler SPLAYED regulates specific stress signaling pathways. PLoS Pathog. 4, 1-8.
Wang, H., Liu, C., Cheng, J. et al. (2016) Arabidopsis flower and embryo developmental genes are repressed in seedlings by different combinations of polycomb group proteins in association with distinct sets of cis-regulatory elements. PLoS Genet. 12, 1-25.
van Wersch, R., Li, X. and Zhang, Y. (2016) Mighty dwarfs: Arabidopsis autoimmune mutants and their usages in genetic dissection of plant immunity. Front. Plant Sci. 7, 1-8.
Wildermuth, M.C., Dewdney, J., Wu, G. and Ausubel, F.M. (2001) Isochorismate synthase is required to synthesize salicylic acid for plant defence. Nature, 414, 562-565.
Wolff, P., Weinhofer, I., Seguin, J. et al. (2011) High-resolution analysis of parent-of-origin allelic expression in the Arabidopsis endosperm. PLoS Genet. 7, e1002126.
Wu, M.-F., Sang, Y., Bezhani, S., Yamaguchi, N., Han, S.-K., Li, Z., Su, Y., Slewinski, T.L. and Wagner, D. (2012) SWI2/SNF2 chromatin remodeling ATPases overcome polycomb repression and control floral organ identity with the LEAFY and SEPALLATA3 transcription factors. Proc. Natl Acad. Sci. 109, 3576-3581.
Wutz, A. (2011) Gene silencing in X-chromosome inactivation: advances in understanding facultative heterochromatin formation. Nat. Rev. Genet. 12, 542-553.
Zhang, X., Germann, S., Blus, B.J., Khorasanizadeh, S., Gaudin, V. and Jacobsen, S.E. (2007) The Arabidopsis LHP1 protein colocalizes with histone H3 Lys27 trimethylation. Nat. Struct. Mol. Biol. 14, 869-871.
Zheng, X.Y., Spivey, N.W., Zeng, W., Liu, P.-P.P., Fu, Z.Q., Klessig, D.F., He, S.Y. and Dong, X. (2012) Coronatine promotes Pseudomonas syringae virulence in plants by activating a signaling cascade that inhibits salicylic acid accumulation. Cell Host Microbe, 11, 587-596.
Zhou, Y., Romero-Campero, F.J., Gómez-Zambrano, Á., Turck, F. and Calonje, M. (2017) H2A monoubiquitination in Arabidopsis thaliana is generally independent of LHP1 and PRC2 activity. Genome Biol. 18, 69.